Advertisement

Protoplasma

pp 1–12 | Cite as

Elevated gibberellin enhances lignin accumulation in celery (Apium graveolens L.) leaves

  • Ao-Qi Duan
  • Kai Feng
  • Guang-long Wang
  • Jie-Xia Liu
  • Zhi-Sheng Xu
  • Ai-Sheng XiongEmail author
Original Article
  • 64 Downloads

Abstract

Gibberellin (GA) is a phytohormone of a biguanide compound that plays an important role throughout the life cycle of a plant. Lignin, a phenylalanine-derived aromatic polymer, can enhance the water transport function and structural resistance of cell walls. This function is also the core on biology of higher terrestrial plants. An appropriate lignin level is important to the quality of leafy vegetables, such as celery. The relationship between gibberellin levels and the occurrence of lignification has not been reported in celery. In this study, the leaf blades and petioles of celery cultivars ‘Liuhe Huangxinqin’ and ‘Jinnan Shiqin’ were used as materials, and different concentrations of exogenous gibberellin were applied to analyze the growth and lignin distribution of leaf blades and petioles. It was found that gibberellin treatment could influence the lignin content in celery leaves. Autofluorescence analysis under ultraviolet (UV) excitation showed that gibberellin treatment caused lignification of celery leaf tissue. The expression profiles of 12 genes related to lignin synthesis changed with the increase of gibberellin concentration. Our results showed that gibberellin played a significant role in the accumulation of lignin in the development of celery leaves. This provides a basis for further study on the regulation of lignin metabolism in plants and exerts a vital part in the application of plant growth regulators to production.

Keywords

Exogenous gibberellin Lignin Development Leaves Apium graveolens L. 

Abbreviations

4CL

4-Coumarate-CoA ligase

C3′H

p-Coumaroyl shikimate/quinate 3′-hydroxylase

C4H

Cinnamate 4-hydroxylase

CAD

Cinnamyl alcohol dehydrogenase

CCR

Cinnamoyl-CoA reductase

CCoAOMT

Caffeoyl-CoA O-methyltransferase

COMT

Caffeic acid O-methyltransferase

F5H

Ferulate 5-hydroxylase

HCT

Hydroxycinnamoyl-CoA shikimate/quinate hydroxycinnamoyl transferase

LAC

Laccase

PAL

Phenylalanine ammonia lyase

PER

Peroxidase

RT-qPCR

Quantitative real-time polymerase chain reaction

GA

Gibberellin

DW

Dry weight

UV

Ultraviolet

Notes

Author contributions

Conceived and designed the experiments: ASX, AQD. Performed the experiments: AQD, KF, JXL, ZSX. Analyzed the data: AQD, KF. Contributed reagents/materials/analysis tools: ASX. Wrote the paper: AQD. Revised the paper: ASX, GLW. All authors read and approved the final manuscript.

Funding information

The research was supported by the Jiangsu Agricultural Science and Technology Innovation Fund [CX(2018)-2007], National Natural Science Foundation of China (31272175), and Priority Academic Program Development of Jiangsu Higher Education Institutions Project (PAPD).

Compliance with ethical standards

Competing interests

The authors declare that they have no conflict of interest.

Supplementary material

709_2018_1341_MOESM1_ESM.xls (32 kb)
ESM 1 (XLS 32 kb)
709_2018_1341_MOESM2_ESM.xls (18 kb)
ESM 2 (XLS 17 kb)

References

  1. Achard P, Gusti A, Cheminant S, Alioua M, Dhondt S, Coppens F, Beemster GT, Genschik P (2009) Gibberellin signaling controls cell proliferation rate in Arabidopsis. Curr Biol 19(14):1188–1193Google Scholar
  2. Biddington NL, Thomas TH (2010) Thermodormancy in celery seeds and its removal by cytokinins and gibberellins. Physiol Plant 42(4):401–405Google Scholar
  3. Biemelt S, Tschiersch H, Sonnewald U (2004) Impact of altered gibberellin metabolism on biomass accumulation, lignin biosynthesis, and photosynthesis in transgenic tobacco plants. Plant Physiol 135(1):254–265Google Scholar
  4. Binenbaum J, Weinstain R, Shani E (2018) Gibberellin localization and transport in plants. Trends Plant Sci 23(5):410–421.  https://doi.org/10.1016/j.tplants.2018.02.005 Google Scholar
  5. Boerjan W, Ralph J, Baucher M (2003) Lignin biosynthesis. Annu Rev Plant Biol 54(1):519–546Google Scholar
  6. Brocklehurst PA, Rankin WEF, Thomas TH (1982) Stimulation of celery seed germination and seedling growth with combined ethephon, gibberellin and polyethylene glycol seed treatments. Plant Growth Regul 1(3):195–202Google Scholar
  7. Buchanan BB, Gruissem W, Jones RL (2000) Biochemistry and molecular biology of plants. Wiley, RockvilleGoogle Scholar
  8. Cervilla LM, Rosales MA, Rubiowilhelmi MM, SáNchezrodríGuez E, Blasco B, RíOs JJ, Romero L, Ruiz JM (2009) Involvement of lignification and membrane permeability in the tomato root response to boron toxicity. Plant Sci 176(4):545–552Google Scholar
  9. Chong, Xu CJ, Li X, Ferguson I, Chen (2006) Accumulation of lignin in relation to change in activities of lignification enzymes in loquat fruit flesh after harvest. Postharvest Biol Technol 40(2):163–169Google Scholar
  10. Dhingra D, Michael M, Rajput H, Patil RT (2012) Dietary fibre in foods: a review. J Food Sci Technol 49(3):255–266.  https://doi.org/10.1007/s13197-011-0365-5 Google Scholar
  11. Doaigey AR, Al-Whaibi MH, Siddiqui MH, Sahli AAA, El-Zaidy ME (2013) Effect of GA3 and 2,4-D foliar application on the anatomy of date palm ( Phoenix dactylifera L.) seedling leaf. Saudi J Biol Sci 20(2):141–147Google Scholar
  12. Donaldson LA (2001) Lignification and lignin topochemistry—an ultrastructural view. Phytochemistry 57(6):859–873Google Scholar
  13. Goldberg-Moeller R, Shalom L, Shlizerman L, Samuels S, Zur N, Ophir R, Blumwald E, Sadka A (2013) Effects of gibberellin treatment during flowering induction period on global gene expression and the transcription of flowering-control genes in Citrus buds. Plant Sci 198:46–57.  https://doi.org/10.1016/j.plantsci.2012.09.012
  14. Israelsson M, Sundberg B, Moritz T (2010) Tissue-specific localization of gibberellins and expression of gibberellin-biosynthetic and signaling genes in wood-forming tissues in aspen. Plant J 44(3):494–504Google Scholar
  15. Itoh H, Tanakaueguchi M, Kawaide H, Chen X, Kamiya Y, Matsuoka M (2010) The gene encoding tobacco gibberellin 3beta-hydroxylase is expressed at the site of GA action during stem elongation and flower organ development. Plant J 20(1):15–24Google Scholar
  16. Jacobsen JV, Pressman E, Pyliotis NA (1976) Gibberellin-induced separation of cells in isolated endosperm of celery seed. Planta 129(2):113–122Google Scholar
  17. Jia XL, Wang GL, Xiong F, Yu XR, Xu ZS, Wang F, Xiong AS (2015) De novo assembly, transcriptome characterization, lignin accumulation, and anatomic characteristics: novel insights into lignin biosynthesis during celery leaf development. Sci Rep 5:8259.  https://doi.org/10.1038/srep08259 Google Scholar
  18. Kay RM (1982) Dietary fiber. J Lipid Res 23(2):221–242Google Scholar
  19. Lattimer JM, Haub MD (2010) Effects of dietary fiber and its components on metabolic health. Nutrients 2(12):1266–1289.  https://doi.org/10.3390/nu2121266 Google Scholar
  20. Li X, Li S, Lin JX (2003) Effect of GA 3 spraying on lignin and auxin contents and the correlated enzyme activities in bayberry ( Myrica rubra Bieb.) during flower-bud induction. Plant Sci 164(4):549–556Google Scholar
  21. Li MY, Feng W, Qian J, Wang GL, Chang T, Xiong AS (2016) Validation and comparison of reference genes for qPCR normalization of celery (Apium graveolens) at different development stages. Front Plant Sci 7:313Google Scholar
  22. Liu JX, Feng K, Wang GL, Xu ZS, Wang F, Xiong AS (2018) Elevated CO2 induces alteration in lignin accumulation in celery (Apium graveolens L.). Plant Physiol Biochem 127:310–319Google Scholar
  23. Matsuoka M (2003) Gibberellin signaling: how do plant cells respond to GA signals? J Plant Growth Regul 22(2):123–125Google Scholar
  24. Mitchum MG, Yamaguchi S, Hanada A, Kuwahara A, Yoshioka Y, Kato T, Tabata SS, Kamiya Y, Sun TP (2006) Distant and overlapping roles of two gibberellin 3-oxidasea in Arabidopsis development. Plant J 45(5):804–818Google Scholar
  25. Peng D, Chen X, Yin Y, Lu K, Yang W, Tang Y, Wang Z (2014) Lodging resistance of winter wheat (Triticum aestivum L.): lignin accumulation and its related enzymes activities due to the application of paclobutrazol or gibberellin acid. Field Crop Res 157(2):1–7Google Scholar
  26. Pfaffl MW (2001) A new mathematical model for relative quantification in real-time RT–PCR. Nucleic Acids Res 29(9):e45–e445Google Scholar
  27. Pressman E, Negbi M (1987) Interaction of daylength and applied gibberellins on stem growth and leaf production in three varieties of celery. J Exp Bot 38(191):968–971Google Scholar
  28. Ragni L, Nieminen K, Pacheco-Villalobos D, Sibout R, Schwechheimer C, Hardtke CS (2011) Mobile gibberellin directly stimulates Arabidopsis hypocotyl xylem expansion. Plant Cell 23(4):1322–1336Google Scholar
  29. Shani E, Weinstain R, Zhang Y, Castillejo C, Kaiserli E, Chory J, Tsien RY, Estelle M (2013) Gibberellins accumulate in the elongating endodermal cells of Arabidopsis root. Pnas 110(12):4834–4839Google Scholar
  30. Shannon P, Markiel A, Ozier O, Baliga NS, Wang JT, Ramage D, Amin N, Schwikowski B, Ideker T (2003) Cytoscape: a software environment for integrated models of biomolecular interaction networks. Genome Res 13(11):2498–2504Google Scholar
  31. Silverstone AL, Sun T (2000) Gibberellins and the green revolution. Trends Plant Sci 5(1):1–2Google Scholar
  32. Sun TP (2010) Gibberellin signal transduction in stem elongation & leaf growth. Springer, NetherlandsGoogle Scholar
  33. Tanimoto E (2005) Regulation of root growth by plant hormones—roles for auxin and gibberellin. Crit Rev Plant Sci 24(4):249–265Google Scholar
  34. Thomas TH (1989) Gibberellin involvement in dormancy-break and germination of seeds of celery (Apium graveolens L.). Plant Growth Regul 8(3):255–261Google Scholar
  35. Trowell H, Burkitt D, Heaton K (1985) Dietary fibre, fibre-depleted foods and disease. Academic Press, London, pp 305–316Google Scholar
  36. Ubedatomás S, Federici F, Casimiro I, Beemster GTS, Bhalerao R, Swarup R, Doerner P, Haseloff J, Bennett MJ (2009) Gibberellin signaling in the endodermis controls Arabidopsis root meristem size. Curr Biol 19(14):1194–1199Google Scholar
  37. Wang GL, Huang Y, Zhang XY, Xu ZS, Wang F, Xiong AS (2016a) Transcriptome-based identification of genes revealed differential expression profiles and lignin accumulation during root development in cultivated and wild carrots. Plant Cell Rep 35(8):1743–1755Google Scholar
  38. Wang GL, Que F, Xu ZS, Wang F, Xiong AS (2016b) Exogenous gibberellin enhances secondary xylem development and lignification in carrot taproot. Protoplasma 254(2):1–10Google Scholar
  39. Yamaguchi S, Smith MW, Brown RG, Kamiya Y, Sun T (1998) Phytochrome regulation and differential expression of gibberellin 3beta-hydroxylase genes in germinating Arabidopsis seeds. Plant Cell 10(12):2115–2126Google Scholar
  40. Yang SL, Zhang XN, Lu GL, Wang CR, Wang R (2015) Regulation of gibberellin on gene expressions related with the lignin biosynthesis in ‘Wangkumbae’ pear (Pyrus pyrifolia Nakai) fruit. Plant Growth Regul 76(2):127–134Google Scholar
  41. Yaxley JR, Ross JJ, Sherriff LJ, Reid JB (2001) Gibberellin biosynthesis mutations and root development in pea. Plant Physiol 125(2):627–633Google Scholar
  42. Zhao Q, Dixon RA (2011) Transcriptional networks for lignin biosynthesis: more complex than we thought? Trends Plant Sci 16(4):227–233Google Scholar
  43. Zhao XY, Zhu DF, Zhou B, Peng WS, Lin JZ, Huang XQ, Re-Qing HE, Zhuo YH, Peng D, Tang DY (2010) Over-expression of the AtGA2ox8 gene decreases the biomass accumulation and lignification in rapeseed (Brassica napus L.). J Zhejiang Univ Sci B (Biomed Biotechnol) 11(7):471–481Google Scholar

Copyright information

© Springer-Verlag GmbH Austria, part of Springer Nature 2019

Authors and Affiliations

  1. 1.State Key Laboratory of Crop Genetics and Germplasm Enhancement, College of HorticultureNanjing Agricultural UniversityNanjingChina

Personalised recommendations